A SEL1L mutation links a canine progressive early-onset cerebellar ataxia to the endoplasmic reticulum-associated protein degradation (ERAD) machinery

PLoS Genetics

Volumn 8, Issue 6, 2012, Pages

  Kyöstilä, Kaisa ^a,b   Cizinauskas, Sigitas ^c   Seppälä, Eija H ^a,b   Suhonen, Esko ^d   Jeserevics, Janis ^c   Sukura, Antti ^a   Syrjä, Pernilla ^a   Lohi, Hannes ^a,b  

^a UNIVERSITY OF HELSINKI   (Finland)

^b FOLKHÄLSAN INSTITUTE OF GENETICS   (Finland)

^c Referral Animal Neurology Hospital Aisti   (Finland)

^d Small Animal Clinic Kontiolahti   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MARKER; CELL PROTEIN; PROTEIN; SEL 1 SUPPRESSOR OF LIN 12 LIKE PROTEIN; SEL1L PROTEIN, HUMAN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL; ANIMAL DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ATROPHY; BRAIN CORTEX; CELL LOSS; CEREBELLAR ATAXIA; CEREBELLUM CORTEX; CHEMISTRY; CHROMOSOME 8; CONTROLLED STUDY; DISEASE MODEL; DOG; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; EXON; EXPERIMENTAL DOG; FAILURE TO THRIVE; FEMALE; GENE EXPRESSION REGULATION; GENE FREQUENCY; GENE LOCUS; GENE MAPPING; GENETIC ASSOCIATION; GENETIC LINKAGE; GENETICS; GENOTYPE; HETEROZYGOTE; HISTOPATHOLOGY; HOMOZYGOSITY; HUMAN; MALE; METABOLISM; MISSENSE MUTATION; MOLECULAR GENETICS; MUTATOR GENE; NERVE DEGENERATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PEDIGREE; PHENOTYPE; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FOLDING; PURKINJE CELL; RADIOGRAPHY; RECESSIVE GENE; SEL 1 SUPPRESSOR OF LIN 12 LIKE GENE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; TREMOR; UPREGULATION;

AMINO ACID SEQUENCE; ANIMALS; CEREBELLAR ATAXIA; CEREBELLAR CORTEX; CHEMISTRY; DISEASE MODELS, ANIMAL; DOGS; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; GENES, RECESSIVE; GENETIC LINKAGE; GENETICS; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HUMANS; METABOLISM; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PATHOLOGY; PEDIGREE; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN FOLDING; PROTEINS; PROTEOLYSIS; RADIOGRAPHY; SEQUENCE ALIGNMENT; VETERINARY;

CANIS FAMILIARIS;

EID: 84875076497     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002759     Document Type: Article

References (105)

1. Taroni F, DiDonato S, (2004) Pathways to motor incoordination: The inherited ataxias. Nat Rev Neurosci 5: 641-655.
2. Manto M, Marmolino D, (2009) Cerebellar ataxias. Curr Opin Neurol 22: 419-29.
3. Matilla-Duenas A, Sanchez I, Corral-Juan M, Davalos A, Alvarez R, et al. (2010) Cellular and molecular pathways triggering neurodegeneration in the spinocerebellar ataxias. Cerebellum 9: 148-66.
4. Harding AE, (1983) Classification of the hereditary ataxias and paraplegias. Lancet 1: 1151-1155.
5. Durr A, (2010) Autosomal dominant cerebellar ataxias: Polyglutamine expansions and beyond. Lancet Neurol 9: 885-894.
6. Klockgether T, (2011) Update on degenerative ataxias. Curr Opin Neurol 24: 339-345.
7. Palau F, Espinos C, (2006) Autosomal recessive cerebellar ataxias. Orphanet J Rare Dis 1: 47.
8. Fogel BL, Perlman S, (2007) Clinical features and molecular genetics of autosomal recessive cerebellar ataxias. Lancet Neurol 6: 245-257.
9. Klockgether T, Paulson H, (2011) Milestones in ataxia. Mov Disord 26: 1134-1141.
10. Vermeer S, van de Warrenburg BP, Willemsen MA, Cluitmans M, Scheffer H, et al. (2011) Autosomal recessive cerebellar ataxias: The current state of affairs. J Med Genet 48: 651-659.
11. De Michele G, Coppola G, Cocozza S, Filla A, (2004) A pathogenetic classification of hereditary ataxias: Is the time ripe? J Neurol 251: 913-922.
12. Grüsser-Cornehls U, Bäurle J, (2001) Mutant mice as a model for cerebellar ataxia. Progress in Neurobiology 63: 489-540.
13. Dusart I, Guenet JL, Sotelo C, (2006) Purkinje cell death: Differences between developmental cell death and neurodegenerative death in mutant mice. Cerebellum 5: 163-173.
14. Lalonde R, Strazielle C, (2007) Spontaneous and induced mouse mutations with cerebellar dysfunctions: Behavior and neurochemistry. Brain Res 1140: 51-74.
15. Tonttila P, Lindberg LA, (1971) [Cerebellar ataxia in a Finnish hurrier] Ett fall av cerebellar ataxi hos finsk stövare (Swedish). Suomen Eläinlääkärilehti 77: 135-138.
16. deLahunta A, Averill DR Jr, (1976) Hereditary cerebellar cortical and extrapyramidal nuclear abiotrophy in Kerry Blue Terriers. J Am Vet Med Assoc 168: 1119-1124.
17. Gill JM, Hewland M, (1980) Cerebellar degeneration in the Border Collie. N Z Vet J 28: 170.
18. Steinberg HS, Troncoso JC, Cork LC, Price DL, (1981) Clinical features of inherited cerebellar degeneration in Gordon Setters. J Am Vet Med Assoc 179: 886-890.
19. Yasuba M, Okimoto K, Iida M, Itakura C, (1988) Cerebellar cortical degeneration in Beagle dogs. Vet Pathol 25: 315-317.
20. Thomas JB, Robertson D, (1989) Hereditary cerebellar abiotrophy in Australian Kelpie dogs. Aust Vet J 66: 301-302.
21. Perille AL, Baer K, Joseph RJ, Carrillo JM, Averill DR, (1991) Postnatal cerebellar cortical degeneration in Labrador Retriever puppies. Can Vet J 32: 619-621.
22. Chieffo C, Stalis IH, Van Winkle TJ, Haskins ME, Patterson DF, (1994) Cerebellar Purkinje's cell degeneration and coat color dilution in a family of Rhodesian Ridgeback dogs. J Vet Intern Med 8: 112-116.
23. Carmichael KP, Miller M, Rawlings CA, Fischer A, Oliver JE, et al. (1996) Clinical, hematologic, and biochemical features of a syndrome in Bernese Mountain Dogs characterized by hepatocerebellar degeneration. J Am Vet Med Assoc 208: 1277-1279.
24. Higgins RJ, LeCouteur RA, Kornegay JN, Coates JR, (1998) Late-onset progressive spinocerebellar degeneration in Brittany Spaniel dogs. Acta Neuropathol 96: 97-101.
25. van Tongern SE, van Vonderen IK, van Nes JJ, van den Ingh TS, (2000) Cerebellar cortical abiotrophy in two Portuguese Podenco littermates. Vet Q 22: 172-174.
26. Steinberg HS, Van Winkle T, Bell JS, de Lahunta A, (2000) Cerebellar degeneration in Old English Sheepdogs. J Am Vet Med Assoc 217: 1162-1165.
27. Sandy JR, Slocombe RF, Mitten RW, Jedwab D, (2002) Cerebellar abiotrophy in a family of Border Collie dogs. Vet Pathol 39: 736-738.
28. Gandini G, Botteron C, Brini E, Fatzer R, Diana A, et al. (2005) Cerebellar cortical degeneration in three English Bulldogs: Clinical and neuropathological findings. J Small Anim Pract 46: 291-294.
29. Flegel T, Matiasek K, Henke D, Grevel V, (2007) Cerebellar cortical degeneration with selective granule cell loss in Bavarian Mountain Dogs. J Small Anim Pract 48: 462-465.
30. Urkasemsin G, Linder KE, Bell JS, de Lahunta A, Olby NJ, (2010) Hereditary cerebellar degeneration in Scottish Terriers. J Vet Intern Med 24: 565-570.
31. de Lahunta A, (1990) Abiotrophy in domestic animals: A review. Can J Vet Res 54: 65-76.
32. Summers BA, Cummings JF, De Lahunta A, (1995) Veterinary neuropathology St. Louis Mosby pp. 300-305.
33. Sisó S, Hanzlíček D, Fluehmann G, Kathmann I, Tomek A, et al. (2006) Neurodegenerative diseases in domestic animals: A comparative review. The Veterinary Journal 171: 20-38.
34. Zeng R, Farias FH, Johnson GS, McKay SD, Schnabel RD, et al. (2011) A truncated retrotransposon disrupts the GRM1 coding sequence in Coton de Tulear dogs with Bandera's Neonatal Ataxia. J Vet Intern Med 25: 267-272.
35. Shearman JR, Cook RW, McCowan C, Fletcher JL, Taylor RM, et al. (2011) Mapping cerebellar abiotrophy in australian kelpies. Anim Genet 42: 675-678.
36. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, et al. (2007) PLINK: A tool set for whole-genome association and population-based linkage analyses. The American Journal of Human Genetics 81: 559-575.
37. Hiekkalinna T, Schaffer AA, Lambert B, Norrgrann P, Goring HH, et al. (2011) PSEUDOMARKER: A powerful program for joint linkage and/or linkage disequilibrium analysis on mixtures of singletons and related individuals. Hum Hered 71: 256-266.
38. Lilley BN, Ploegh HL, (2005) Multiprotein complexes that link dislocation, ubiquitination, and extraction of misfolded proteins from the endoplasmic reticulum membrane. Proc Natl Acad Sci U S A 102: 14296-14301.
39. Mueller B, Lilley BN, Ploegh HL, (2006) SEL1L, the homologue of yeast Hrd3p, is involved in protein dislocation from the mammalian ER. J Cell Biol 175: 261-270.
40. Christianson JC, Shaler TA, Tyler RE, Kopito RR, (2008) OS-9 and GRP94 deliver mutant alpha1-antitrypsin to the Hrd1-SEL1L ubiquitin ligase complex for ERAD. Nat Cell Biol 10: 272-282.
41. Mueller B, Klemm EJ, Spooner E, Claessen JH, Ploegh HL, (2008) SEL1L nucleates a protein complex required for dislocation of misfolded glycoproteins. Proc Natl Acad Sci U S A 105: 12325-12330.
42. Ross CA, Poirier MA, (2004) Protein aggregation and neurodegenerative disease. Nat Med 10 (Suppl): S10-7.
43. Tai HC, Schuman EM, (2008) Ubiquitin, the proteasome and protein degradation in neuronal function and dysfunction. Nat Rev Neurosci 9: 826-838.
44. Martina JA, Bonangelino CJ, Aguilar RC, Bonifacino JS, (2001) Stonin 2: An adaptor-like protein that interacts with components of the endocytic machinery. J Cell Biol 153: 1111-1120.
45. Walther K, Diril MK, Jung N, Haucke V, (2004) Functional dissection of the interactions of stonin 2 with the adaptor complex AP-2 and synaptotagmin. Proc Natl Acad Sci U S A 101: 964-969.
46. Diril MK, Wienisch M, Jung N, Klingauf J, Haucke V, (2006) Stonin 2 is an AP-2-dependent endocytic sorting adaptor for synaptotagmin internalization and recycling. Dev Cell 10: 233-244.
47. Jung N, Wienisch M, Gu M, Rand JB, Muller SL, et al. (2007) Molecular basis of synaptic vesicle cargo recognition by the endocytic sorting adaptor stonin 2. J Cell Biol 179: 1497-1510.
48. Biunno I, Castiglioni B, Rogozin IB, DeBellis G, Malferrari G, et al. (2002) Cross-species conservation of SEL1L, a human pancreas-specific expressing gene. OMICS 6: 187-198.
49. Biunno I, Cattaneo M, Orlandi R, Canton C, Biagiotti L, et al. (2006) SEL1L a multifaceted protein playing a role in tumor progression. J Cell Physiol 208: 23-38.
50. Biunno I, Bernard L, Dear P, Cattaneo M, Volorio S, et al. (2000) SEL1L, the human homolog of C. elegans sel-1: Refined physical mapping, gene structure and identification of polymorphic markers. Hum Genet 106: 227-235.
51. Zhao L, Ackerman SL, (2006) Endoplasmic reticulum stress in health and disease. Curr Opin Cell Biol 18: 444-452.
52. Matus S, Glimcher LH, Hetz C, (2011) Protein folding stress in neurodegenerative diseases: A glimpse into the ER. Curr Opin Cell Biol 23: 239-252.
53. Zhang K, Kaufman RJ, (2006) The unfolded protein response: A stress signaling pathway critical for health and disease. Neurology 66: S102-9.
54. Malhotra JD, Kaufman RJ, (2007) The endoplasmic reticulum and the unfolded protein response. Semin Cell Dev Biol 18: 716-731.
55. Vembar SS, Brodsky JL, (2008) One step at a time: Endoplasmic reticulum-associated degradation. Nat Rev Mol Cell Biol 9: 944-957.
56. Walter P, Ron D, (2011) The unfolded protein response: From stress pathway to homeostatic regulation. Science 334: 1081-1086.
57. Hetz C, (2012) The unfolded protein response: Controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol 13: 89-102.
58. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, et al. (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415: 92-96.
59. Acosta-Alvear D, Zhou Y, Blais A, Tsikitis M, Lents NH, et al. (2007) XBP1 controls diverse cell type- and condition-specific transcriptional regulatory networks. Mol Cell 27: 53-66.
60. Yamamoto K, Sato T, Matsui T, Sato M, Okada T, et al. (2007) Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6alpha and XBP1. Dev Cell 13: 365-376.
61. Biunno I, Appierto V, Cattaneo M, Leone BE, Balzano G, et al. (1997) Isolation of a pancreas-specific gene located on human chromosome 14q31: Expression analysis in human pancreatic ductal carcinomas. Genomics 46: 284-286.
62. Donoviel DB, Donoviel MS, Fan E, Hadjantonakis A-, Bernstein A, (1998) Cloning and characterization of sel-1l, a murine homolog of the C. elegans sel-1 gene. Mech Dev 78: 203-207.
63. Meusser B, Hirsch C, Jarosch E, Sommer T, (2005) ERAD: The long road to destruction. Nat Cell Biol 7: 766-772.
64. Hirsch C, Gauss R, Horn SC, Neuber O, Sommer T, (2009) The ubiquitylation machinery of the endoplasmic reticulum. Nature 458: 453-460.
65. Hosokawa N, Wada I, Nagasawa K, Moriyama T, Okawa K, et al. (2008) Human XTP3-B forms an endoplasmic reticulum quality control scaffold with the HRD1-SEL1L ubiquitin ligase complex and BiP. J Biol Chem 283: 20914-20924.
66. Cormier JH, Tamura T, Sunryd JC, Hebert DN, (2009) EDEM1 recognition and delivery of misfolded proteins to the SEL1L-containing ERAD complex. Mol Cell 34: 627-633.
67. Riemer J, Appenzeller-Herzog C, Johansson L, Bodenmiller B, Hartmann-Petersen R, et al. (2009) A luminal flavoprotein in endoplasmic reticulum-associated degradation. Proc Natl Acad Sci U S A 106: 14831-14836.
68. Lindholm D, Wootz H, Korhonen L, (2006) ER stress and neurodegenerative diseases. Cell Death Differ 13: 385-392.
69. Kim I, Xu W, Reed JC, (2008) Cell death and endoplasmic reticulum stress: Disease relevance and therapeutic opportunities. Nat Rev Drug Discov 7: 1013-1030.
70. Kaneko M, Nomura Y, (2003) ER signaling in unfolded protein response. Life Sci 74: 199-205.
71. Matsumoto M, Minami M, Takeda K, Sakao Y, Akira S, (1996) Ectopic expression of CHOP (GADD153) induces apoptosis in M1 myeloblastic leukemia cells. FEBS Lett 395: 143-147.
72. Zinszner H, Kuroda M, Wang X, Batchvarova N, Lightfoot RT, et al. (1998) CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 12: 982-995.
73. Oyadomari S, Mori M, (2004) Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 11: 381-389.
74. Ron D, Habener JF, (1992) CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP and functions as a dominant-negative inhibitor of gene transcription. Genes Dev 6: 439-453.
75. Okada T, Yoshida H, Akazawa R, Negishi M, Mori K, (2002) Distinct roles of activating transcription factor 6 (ATF6) and double-stranded RNA-activated protein kinase-like endoplasmic reticulum kinase (PERK) in transcription during the mammalian unfolded protein response. Biochem J 366: 585-594.
76. Saltini G, Dominici R, Lovati C, Cattaneo M, Michelini S, et al. (2006) A novel polymorphism in SEL1L confers susceptibility to alzheimer's disease. Neurosci Lett 398: 53-58.
77. Francisco AB, Singh R, Li S, Vani AK, Yang L, et al. (2010) Deficiency of suppressor enhancer Lin12 1 like (SEL1L) in mice leads to systemic endoplasmic reticulum stress and embryonic lethality. J Biol Chem 285: 13694-13703.
78. Mittl PRE, Schneider-Brachert W, (2007) Sel1-like repeat proteins in signal transduction. Cell Signal 19: 20-31.
79. Iida Y, Fujimori T, Okawa K, Nagata K, Wada I, et al. (2011) SEL1L protein critically determines the stability of the HRD1-SEL1L endoplasmic reticulum-associated degradation (ERAD) complex to optimize the degradation kinetics of ERAD substrates. J Biol Chem 286: 16929-16939.
80. Harada Y, Ozaki K, Suzuki M, Fujiwara T, Takahashi E, et al. (1999) Complete cDNA sequence and genomic organization of a human pancreas-specific gene homologous to caenorhabditis elegans sel-1. J Hum Genet 44: 330-336.
81. Cattaneo M, Lotti LV, Martino S, Cardano M, Orlandi R, et al. (2009) Functional characterization of two secreted SEL1L isoforms capable of exporting unassembled substrate. J Biol Chem 284: 11405-11415.
82. Cattaneo M, Lotti LV, Martino S, Alessio M, Conti A, et al. (2011) Secretion of novel SEL1L endogenous variants is promoted by ER stress/UPR via endosomes and shed vesicles in human cancer cells. PLoS ONE 6: e17206 10.1371/journal.pone.0017206.
83. Klockgether T, Evert B, (1998) Genes involved in hereditary ataxias. Trends Neurosci 21: 413-418.
84. Lim J, Hao T, Shaw C, Patel AJ, Szabó G, et al. (2006) A Protein-Protein interaction network for human inherited ataxias and disorders of purkinje cell degeneration. Cell 125: 801-814.
85. Anttonen AK, Mahjneh I, Hamalainen RH, Lagier-Tourenne C, Kopra O, et al. (2005) The gene disrupted in marinesco-sjogren syndrome encodes SIL1, an HSPA5 cochaperone. Nat Genet 37: 1309-1311.
86. Senderek J, Krieger M, Stendel C, Bergmann C, Moser M, et al. (2005) Mutations in SIL1 cause marinesco-sjogren syndrome, a cerebellar ataxia with cataract and myopathy. Nat Genet 37: 1312-1314.
87. Zhao L, Longo-Guess C, Harris BS, Lee JW, Ackerman SL, (2005) Protein accumulation and neurodegeneration in the woozy mutant mouse is caused by disruption of SIL1, a cochaperone of BiP. Nat Genet 37: 974-979.
88. Zhao L, Rosales C, Seburn K, Ron D, Ackerman SL, (2010) Alteration of the unfolded protein response modifies neurodegeneration in a mouse model of marinesco-sjogren syndrome. Hum Mol Genet 19: 25-35.
89. Lee JW, Beebe K, Nangle LA, Jang J, Longo-Guess CM, et al. (2006) Editing-defective tRNA synthetase causes protein misfolding and neurodegeneration. Nature 443: 50-55.
90. Kyuhou S, Kato N, Gemba H, (2006) Emergence of endoplasmic reticulum stress and activated microglia in purkinje cell degeneration mice. Neurosci Lett 396: 91-96.
91. Kitao Y, Hashimoto K, Matsuyama T, Iso H, Tamatani T, et al. (2004) ORP150/HSP12A regulates purkinje cell survival: A role for endoplasmic reticulum stress in cerebellar development. J Neurosci 24: 1486-1496.
92. Wang M, Ye R, Barron E, Baumeister P, Mao C, et al. (2010) Essential role of the unfolded protein response regulator GRP78/BiP in protection from neuronal apoptosis. Cell Death Differ 17: 488-498.
93. Omura T, Kaneko M, Tabei N, Okuma Y, Nomura Y, (2008) Immunohistochemical localization of a ubiquitin ligase HRD1 in murine brain. J Neurosci Res 86: 1577-1587.
94. Kent WJ, (2002) BLAT-the BLAST-like alignment tool. Genome Res 12: 656-664.
95. Oetting WS, Lee HK, Flanders DJ, Wiesner GL, Sellers TA, et al. (1995) Linkage analysis with multiplexed short tandem repeat polymorphisms using infrared fluorescence and M13 tailed primers. Genomics 30: 450-458.
96. Finn RD, Mistry J, Tate J, Coggill P, Heger A, et al. (2010) The pfam protein families database. Nucleic Acids Res 38: D211-22.
97. Schultz J, Milpetz F, Bork P, Ponting CP, (1998) SMART, a simple modular architecture research tool: Identification of signaling domains. Proc Natl Acad Sci U S A 95: 5857-5864.
98. Letunic I, Doerks T, Bork P, (2009) SMART 6: Recent updates and new developments. Nucleic Acids Res 37: D229-32.
99. Thomas PD, Campbell MJ, Kejariwal A, Mi H, Karlak B, et al. (2003) PANTHER: A library of protein families and subfamilies indexed by function. Genome Res 13: 2129-2141.
100. Thomas PD, Kejariwal A, (2004) Coding single-nucleotide polymorphisms associated with complex vs. mendelian disease: Evolutionary evidence for differences in molecular effects. Proc Natl Acad Sci U S A 101: 15398-15403.
101. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, et al. (2010) A method and server for predicting damaging missense mutations. Nat Methods 7: 248-249.
102. Ng PC, Henikoff S, (2001) Predicting deleterious amino acid substitutions. Genome Res 11: 863-874.
103. Ng PC, Henikoff S, (2003) SIFT: Predicting amino acid changes that affect protein function. Nucleic Acids Res 31: 3812-3814.
104. Kumar P, Henikoff S, Ng PC, (2009) Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protoc 4: 1073-1081.
105. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25: 402-408.